Origins and passenger facilities

Passenger facilities were added in 1938. These were used until further investment made Prestwick compatible with jet transportation. The October 1946 USAAF diagram shows a 6,600-foot (2,000-metre) runway 14/32, with a 4,500 ft (1,400 m) runway 8/26 crossing just west of its midpoint. In 1958, runway 13/31 was 7,000 ft (2,100 m) long; in May 1960, the runway's extension to 9,800 ft (3,000 m) opened.

A parallel taxiway, link road and an all-new terminal building were opened by the Queen Mother in 1964. The extension of runway 13/31 caused considerable disruption to road users, for the main road from Monkton into Prestwick now crossed the tarmac of the runway. This was controlled by a "level crossing" system until a new perimeter road was completed.

Military use

In the Second World War the RAF controlled trans-Atlantic flights from Prestwick.

Until February 2016, part of the Prestwick site was occupied by the Royal Navy Fleet Air Arm with RNAS Prestwick, officially known by the Royal Navy as HMS Gannet, where a detachment of three Sea Kings provided a search and rescue role, covering one of the largest SAR areas of the UK including Ben Nevis, the Lakes, Northern Ireland and 200 nautical miles (370 kilometres) past the Irish coast. Additionally, Gannet SAR provided a medical evacuation service to the Scottish island communities. Personnel at the base numbered 15 officers, 11 ratings, 28 civil servants and 50 civilian staff. The crews regularly featured as part of the popular Channel 5 documentary series Highland Emergency. In 2009, the unit broke a new record as they were tasked to 447 call-outs, 20% of the UK's total military SAR call outs for 2009 and making them, for the second year in succession, the busiest search and rescue base in the UK.

There was controversy over the airport's use in the CIA's extraordinary rendition flights, as aircraft had used the airport as a stop-over point. Since November 2013, when the Scottish government took control of the facility, service contracts have been established with the USAF, USN, USMC, Defense Logistics Agency and National Guard.

Glasgow Prestwick Airport is the only place in the United Kingdom where Elvis Presley (who had distant Scottish ancestry) was known to have set foot, when the United States Air Force transport plane carrying him home to the United States stopped to refuel in 1960, en route from West Germany. However, on 21 April 2008, during a BBC Radio 2 interview with Ken Bruce, theatre impresario and chairman of Everton FC, Bill Kenwright, said that Elvis actually spent a day in the UK being shown around London by Tommy Steele in 1958.

Commercial use

In 1945, American Overseas Airlines began regular transatlantic commercial flights began between Prestwick and New York. AOA was later acquired by Pan Am, which used Prestwick as a stop between Europe and North America into the 1970s. BOAC also used Prestwick as a stop between London and New York in the late 1940s and 1950s.

In the 1980s, Prestwick continued to see scheduled transatlantic flights by Air Canada and Northwest Airlines. These carriers both moved their operations to Glasgow Airport after government restrictions were lifted in 1990. Until 1990, the British government required all transatlantic flights to and from Scotland to use Prestwick.